Autophagy is required for self-incompatible pollen rejection in two transgenic <i>Arabidopsis thaliana</i> accessions

MacGregor, Stuart; Lee, Hyun Kyung; Nelles, Hayley; Johnson, Daniel; Zhang, Tong; Ma, Chaozhi; Goring, Daphne R.

doi:10.1093/plphys/kiac026

Cited by 15 publications

(14 citation statements)

References 54 publications

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“…Sporophytic self-incompatibility in Brassicaceae is based on the recognition between the pistil receptor (SRK, S receptor kinase) and pollen ligand (SP11/SCR, S -locus protein 11/ S -locus cysteine-rich protein), which initiates a kinase cascade inhibiting pollen tube growth involving autophagy (Fig. 2 ) (Suzuki et al 1999 ; Schopfer et al 1999 ; Takayama et al 2000 ; Takasaki et al 2000 ; Kusaba et al 2001 ; Macgregor et al 2022 ). SRK/SCR based self-incompatibility is ancient and most probably ancestral to all Brassicaceae (Fobis-Loisy et al 2004 ).…”

Section: Sporophytic Self-incompatibility In Brassicaceaementioning

confidence: 99%

Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae

2022

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Self-incompatibility systems based on self-recognition evolved in hermaphroditic plants to maintain genetic variation of offspring and mitigate inbreeding depression. Despite these benefits in diploid plants, for polyploids who often face a scarcity of mating partners, self-incompatibility can thwart reproduction. In contrast, self-compatibility provides an immediate advantage: a route to reproductive viability. Thus, diploid selfing lineages may facilitate the formation of new allopolyploid species. Here, we describe the mechanism of establishment of at least four allopolyploid species in Brassicaceae (Arabidopsis suecica, Arabidopsis kamchatica, Capsella bursa-pastoris, and Brassica napus), in a manner dependent on the prior loss of the self-incompatibility mechanism in one of the ancestors. In each case, the degraded S-locus from one parental lineage was dominant over the functional S-locus of the outcrossing parental lineage. Such dominant loss-of-function mutations promote an immediate transition to selfing in allopolyploids and may facilitate their establishment.

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Section: Sporophytic Self-incompatibility In Brassicaceaementioning

confidence: 99%

Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae

2022

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“…Since AlPUB17 was also previously found to interact with AlSRK 1 (Indriolo and Goring, 2016), PUB17 and PUB16 were selected to investigate if they functioned in the transgenic A. thaliana SI pathway. The transgenic A. thaliana Al SCR Al SRK C24 line (SI-C24 #15-1) was selected for this study as it displays a strong and stable SI phenotype (Iwano et al ., 2015, Macgregor et al ., 2022). PUB17 and PUB16 are expressed across a broad range of tissues in A. thaliana including the stigma (Klepikova et al ., 2016), and the expression of PUB17 and PUB16 in pistil tissue was confirmed by RT-PCR (Figure 2a).…”

Section: Resultsmentioning

confidence: 99%

“…Previously we found a positive interaction between AlSRK 1 and AlPUB17 (Indriolo and Goring, 2016), and our phylogenetic analysis showed that PUB17 and PUB16 are the two most closely related UND-PUBs to AlARC1 (Figure 1; Indriolo et al ., 2012). The CRISPR/Cas9 system was used to generate pub17 and pub16 mutations in the C24 accession (Figure 2), and these mutations were then crossed into the transgenic A. thaliana SI-C24 line which carries the Al SCR b and Al SRK b transgenes and displays a strong SI phenotype (Iwano et al ., 2015, Macgregor et al ., 2022). Our experiments provided a thorough examination on the requirement of PUB17 and PUB16 at three different stages that are impacted by SI pollen rejection: pollen hydration, pollen tube growth, and seed yield.…”

Section: Discussionmentioning

confidence: 99%

“…In Arabidopsis species, identifying SRK interacting proteins has proven to be more elusive, but some downstream cellular responses following SI pollen perception have been uncovered (Safavian and Goring, 2013, Indriolo et al ., 2014, Iwano et al ., 2015, Macgregor and Goring, 2022, Macgregor et al ., 2022). While A. thaliana carries pseudogenized SCR, SRK , and ARC1 genes, the SI trait can be reinstated using transgenes from SI Arabidopsis species such as A. lyrata and A. halleri (Nasrallah et al ., 2004, Boggs et al ., 2009b, Indriolo et al ., 2014, Iwano et al ., 2015, Zhang et al ., 2019, Rozier et al ., 2020).…”

Section: Introductionmentioning

confidence: 99%

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Investigating a role forPUB17andPUB16in the self-incompatibility pathway in transgenicArabidopsis thaliana

Beronilla,

Goring

2023

Preprint

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In Brassicaceae self-incompatibility (SI), self-pollen rejection is initiated by the S-haplotype specific interactions between the pollen SCR/SP11 ligand and the stigma S Receptor kinase (SRK). In Brassica SI, a member of the Plant U-Box (PUB) E3 ubiquitin ligases, ARC1, is then activated by SRK in this stigma and cellular events downstream of this cause SI pollen rejection by inhibiting pollen hydration and pollen tube growth. During the transition to selfing, Arabidopsis thaliana lost the SI components, SCR, SRK, and ARC1. However, this trait can be reintroduced into A. thaliana by adding back functional copies of these genes from closely related SI species. Both SCR and SRK are required for this, though the degree of SI pollen rejection varies between accessions, and ARC1 is not always needed to produce a strong SI response. For A. thaliana C24, only transforming with A. lyrata SCR and SRK confers a strong SI trait, and so here we investigated if ARC1-related PUBs were involved in the SI pathway. Two close ARC1 paralogs, PUB17 and PUB16, were selected, and CRISPR/Cas9 technology was used to generate pub17 and pub16 mutations in the C24 accession. These mutants were then crossed into a transgenic A. thaliana SI-C24 line and their potential impact on SI pollen rejection was investigated. Overall, we did not observe any significant differences to implicate PUB17 and PUB16 functioning in the transgenic A. thaliana SI-C24 stigma to reject SI pollen.

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“…Recent evidence has shown that autophagy is involved in multiple steps of sexual reproduction, depending on plant species, including male gametophyte development and maturation, self-incompatible pollen rejection and pollen germination (Harrison-Lowe and Olsen, 2008; Kurusu et al, 2014; Li et al, 2020; Norizuki et al, 2020; Zhao et al, 2020; Zhou et al, 2021; Macgregor et al, 2022). Nevertheless, the role(s) of canonical autophagy during sexual reproduction in Arabidopsis thaliana is still an enigma since almost all of the autophagy-defective Arabidopsis mutants such as atg2 , atg5 and atg7 exhibit normal life cycles without any deleterious phenotypes during fertilization, embryogenesis and seed formation.…”

Section: Discussionmentioning

confidence: 99%

ATG5- and ATG7-mediated autophagy regulates pollen tube guidance and male fertility in Arabidopsis thaliana

He¹,

Du²,

Yang³

et al. 2022

Preprint

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Autophagy functions as a crucial cellular scavenger by targeting cytoplasmic cargo to specific lysosome/vacuole for degradation. Autophagy-related (ATG) core proteins including ATG5 and ATG7 are evolutionarily conserved factors that are spatiotemporally orchestrated to regulate multiple processes of autophagy in yeast, mammalian and plant cells. However, autophagy is believed to be functionally dispensable in Arabidopsis thaliana since severe defects during plant growth, development and reproduction have not been observed in most of the ATG loss-of-function mutants, including atg5 and atg7, under standard cultivation conditions. In this study, we report that autophagy does in fact play roles in regulating pollen tube growth guidance and male fertility in Arabidopsis thaliana. A detailed re-assessment of atg5 and atg7 mutants revealed greatly reduced autophagy activity in germinated pollens and the seed formation within siliques is partially abolished. Next, we demonstrated that both the pollen germination ratio and pollen tube length of the mutants decreased at the beginning of germination by time-lapse tracking of pollen germination in vitro and in vivo. Additionally, we observed occurrences of pollen tube twisting and stacking during their growth towards the ovules. Finally, we found abnormal pollen grains containing only a single sperm cell or an undivided generative nucleus. Collectively, these results indicate that ATG5- and ATG7-mediated autophagy is functionally involved in regulating pollen germination, tube growth guidance and sperm cell development in Arabidopsis thaliana.

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Autophagy is required for self-incompatible pollen rejection in two transgenic Arabidopsis thaliana accessions

Cited by 15 publications

References 54 publications

Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae

Ancestral self-compatibility facilitates the establishment of allopolyploids in Brassicaceae

Investigating a role forPUB17andPUB16in the self-incompatibility pathway in transgenicArabidopsis thaliana

ATG5- and ATG7-mediated autophagy regulates pollen tube guidance and male fertility in Arabidopsis thaliana

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